The title character in Chocobo's Mysterious Dungeon is a yellow chocobo named Poulet(プーレ, Pūre?) (a pun on the Japanese "pureiyā" meaning "player" and the French word "poulet" meaning "chicken"), but the player can rename him. Poulet is accompanied by his moogle traveling companion, Atla.

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Chocobo's Mysterious Dungeon borrows many of its game play elements from the Mystery Dungeon sub-genre of rogue-like RPGs. Dungeon layouts are randomly generated, along with the appearance of enemies and items. Items discovered by the player are initially unidentified and may be cursed or otherwise have adverse effects when used or equipped. Equipment found by the player can be upgraded through a system of forging two pieces together, with or without nuts that fuse special effects.

The game's village is the only other area explored by the player, and acts as a central hub for buying and selling items as well as interacting with NPCs. As a result of various events during the game, the village gradually undergoes development, making room for several new housing areas and NPCs who occupy them. Development of the village mostly occurs as a result of the player selling various quantities of items to shops. For instance, selling several Toad cards will eventually cause toads to appear in the village pond.

Movement across dungeon floors occurs on a real-time basis, but attacks are executed by first charging an ATB gauge. An attack can be executed before the ATB gauge is fully charged, but doing so results in a weaker version of the attack. The player's growth is based on an experience level system in which defeating enemies and accumulating experience points will eventually raise the player's status attributes. (i.e. HP, Stamina, etc.)

Each type of magic spell has its own independent level, which only increases as a result of casting that spell X number of times. The player may also find various items (e.g. nuts or cards) that directly raise experience levels, spell levels, HP or Stamina.

A moogle named Atla (アトラ, Atora?) travels with Poulet to a small village. Here, a chocobo villager is possessed by an evil crystal after accidentally unearthing the artifact while tiling his field. The possessed chocobo exiles Poulet into a strange dungeon whose layout and enemies are randomly generated.

Upon reaching the farthest regions of the dungeon's depths, Poulet confronts the possessed chocobo and manages to free him from the crystal's possession, only to see Atla in turn possessed by it. Atla is later saved by Poulet and Chubby Chocobo, who proceed to destroy the crystal altogether. Chocobo and Atla leave the village in search of new adventures, although the player may continue freely exploring bonus dungeons after the story has ended.